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Complex archaea that bridge the gap between prokaryotes and eukaryotes

Abstract

The origin of the eukaryotic cell remains one of the most contentious puzzles in modern biology. Recent studies have provided support for the emergence of the eukaryotic host cell from within the archaeal domain of life, but the identity and nature of the putative archaeal ancestor remain a subject of debate. Here we describe the discovery of ‘Lokiarchaeota’, a novel candidate archaeal phylum, which forms a monophyletic group with eukaryotes in phylogenomic analyses, and whose genomes encode an expanded repertoire of eukaryotic signature proteins that are suggestive of sophisticated membrane remodelling capabilities. Our results provide strong support for hypotheses in which the eukaryotic host evolved from a bona fide archaeon, and demonstrate that many components that underpin eukaryote-specific features were already present in that ancestor. This provided the host with a rich genomic ‘starter-kit’ to support the increase in the cellular and genomic complexity that is characteristic of eukaryotes.

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Figure 1: Identification of a novel archaeal lineage.
Figure 2: Metagenomic reconstruction and phylogenetic analysis of Lokiarchaeum.
Figure 3: Identification and phylogeny of small GTPases and actin orthologues.
Figure 4: Identification of ESCRT components in the Lokiarchaeum genome.
Figure 5: The complex archaeal ancestry of eukaryotes.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

NCBI Reference Sequence

Sequence Read Archive

Data deposits

Sequence data have been deposited to the NCBI Sequence Read Archive under study number SRP045692, which includes 16 rRNA reads (experiment number SRX872366). Protein sequences of Loki2/3 were deposited to GenBank under accession numbers KP869578KP869724. The Lokiarchaeum genome bin and the LCGC14 metagenome projects have been deposited at DDBJ/EMBL/GenBank under the accessions JYIM00000000 and LAZR00000000, respectively. The versions described in this paper are versions JYIM01000000 and LAZR01000000.

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Acknowledgements

We dedicate this paper to the memory of Rolf Bernander. We thank P. Offre and I. de Bruijn for technical advice and useful discussions, and A. Denny for image processing. We also acknowledge the help from chief scientist R. B. Pedersen, the scientific party and the entire crew on board the Norwegian research vessel G.O. Sars during the summer 2010 expedition. All sequencing was performed by the National Genomics Infrastructure sequencing platforms at the Science for Life Laboratory at Uppsala University, a national infrastructure supported by the Swedish Research Council (VR-RFI) and the Knut and Alice Wallenberg Foundation. We thank the Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX) at Uppsala University and the Swedish National Infrastructure for Computing (SNIC) at the PDC Center for High-Performance Computing for providing computational resources. This work was supported by grants of the Swedish Research Council (VR grant 621-2009-4813), the European Research Council (ERC Starting grant 310039-PUZZLE_CELL) and the Swedish Foundation for Strategic Research (SSF-FFL5) to T.J.G.E., and by grants of the Carl Tryggers Stiftelse för Vetenskaplig Forskning (to A.S.), the Wenner-Gren Stiftelserna (to J.H.S.), and by Marie Curie IIF (331291 to J.H.S.) and IEF (625521 to A.S.) grants by the European Union. S.L.J received financial support from the H2DEEP project through the EuroMARC program, and by the Research Council of Norway through the Centre for Geobiology, University of Bergen. C.S. is supported by the Austrian Science Fund (FWF grant P27017).

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T.J.G.E., S.L.J. and C.S. conceived the study. S.L.J. provided deep-sea sediments and isolated community DNA. R.v.E., J.H.S. and A.E.L. prepared sequencing libraries. A.E.L., J.H.S., S.L.J. and J.M. analysed environmental sequence data. L.G., K.Z.-N. and J.H.S. performed, optimised and analysed metagenomic sequence assemblies. L.G., J.H.S., A.S., K.Z.-N. and T.J.G.E. analysed genomic data and performed phylogenetic analyses. A.S., L.G., S.L.J. and T.J.G.E analysed genomic signatures of DSAG. T.J.G.E., A.S., S.L.J. and L.G. wrote, and all authors edited and approved the manuscript.

Corresponding authors

Correspondence to Lionel Guy or Thijs J. G. Ettema.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Table 1 Overview of Lokiarchaeal ESPs

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This file contains a Supplementary Discussion detailing the phylogenetic analysis of the Lokiarchaeota-Eukarya affiliation as well as the simplified ‘eukaryotic ribosome’ of Lokiarchaeum. It also includes Supplementary Tables 1-10 and Supplementary Figures 1-24, which provide more details into annotations, applied methods and phylogenetic analyses. (PDF 5532 kb)

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Spang, A., Saw, J., Jørgensen, S. et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521, 173–179 (2015). https://doi.org/10.1038/nature14447

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